How nematode sperm crawl

Author:

Bottino Dean1,Mogilner Alexander2,Roberts Tom3,Stewart Murray4,Oster George1

Affiliation:

1. Department of Molecular and Cellular Biology, University of California, Berkeley, CA 94720-3112, USA

2. Department of Mathematics, University of California, Davis, CA 95616, USA

3. Department of Biological Science, Florida State University, Tallahassee, FL 32306-3050, USA

4. MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, England

Abstract

Sperm of the nematode, Ascaris suum, crawl using lamellipodial protrusion, adhesion and retraction, a process analogous to the amoeboid motility of other eukaryotic cells. However, rather than employing an actin cytoskeleton to generate locomotion, nematode sperm use the major sperm protein (MSP). Moreover, nematode sperm lack detectable molecular motors or the battery of actin-binding proteins that characterize actin-based motility. The Ascaris system provides a simple ‘stripped down’ version of a crawling cell in which to examine the basic mechanism of cell locomotion independently of other cellular functions that involve the cytoskeleton. Here we present a mechanochemical analysis of crawling in Ascaris sperm. We construct a finite element model wherein (a) localized filament polymerization and bundling generate the force for lamellipodial extension and (b) energy stored in the gel formed from the filament bundles at the leading edge is subsequently used to produce the contraction that pulls the rear of the cell forward. The model reproduces the major features of crawling sperm and provides a framework in which amoeboid cell motility can be analyzed. Although the model refers primarily to the locomotion of nematode sperm, it has important implications for the mechanics of actin-based cell motility.Movies available on-line.

Publisher

The Company of Biologists

Subject

Cell Biology

Reference62 articles.

1. Abercrombie, M. (1980). The Croonian lecture, 1978. The crawling movement of metazoan cells. Proc. Roy. Soc. Lond. B207, 129-147.

2. Bergethon, P. R. (1998). The Physical Basis Of Biochemistry: The Foundations Of Molecular Biophysics. New York: Springer.

3. Blanchoin, L., Pollard, T. and Mullins, R. (2000). Interactions of ADF/cofilin, Arp2/3 complex, capping protein and profilin in remodeling of branched actin filament networks. Curr. Biol.10, 1273-1282.

4. Borisy, G. and Svitkina, T. (2000). Actin machinery: pushing the envelope. Curr. Opin. Cell Biol.12, 104-112.

5. Bottino, D. (2001). Computer simulations of mechanochemical coupling in a deforming domain: Applications to cell motion. In IMA Frontiers in Applications of Mathematics: Mathematical Models for Biological Pattern Formation, pp. 295. New York: Springer.

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